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Integrating circadian dynamics with physiological processes in plants

A Corrigendum to this article was published on 13 October 2015

This article has been updated

Key Points

  • The plant circadian clock comprises multiple interlocked feedback loops and features transcriptional, post-transcriptional (alternative splicing) and post-translational regulation of protein stability, activity and localization. The complexity and interdigitation of the feedback loops with environmental input pathways and output pathways argues persuasively in favour of a network consideration of the circadian system.

  • Circadian regulation of PHYTOCHROME-INTERACTING FACTOR (PIF) transcription together with PHYTOCHROME B (PHYB)-mediated degradation of PIF proteins in the light 'gates' hypocotyl elongation to the late night. This provides an example of external coincidence of light with clock-derived oscillations to impart temporal and environmental sensitivity to growth control.

  • Day length is measured in the leaves via a complex network and results in expression of FLOWERING LOCUS T (FT), which is subsequently transmitted to the shoot apical meristem, where it complexes with FD to induce floral meristem identity (FMI) genes

  • Responses to abiotic stresses are energetically costly, so plants use the circadian clock to temporally restrict both the basal expression and the induction of response pathways to multiple abiotic stresses, including drought and cold. The timing of the response is coordinated with the normal temporal organization of metabolism and physiology to minimize metabolic incompatibilities and competition for limiting substrates and to maximize the efficiency and effectiveness of the response.

  • As with responses to abiotic stresses, constitutive expression of defence pathways that confer resistance to pathogens and herbivores is deleterious. Plants use the circadian clock to temporally restrict both the basal expression and the induction of defence pathways to the time of day when the threat posed by pathogens and herbivores is maximal, thereby minimizing this fitness cost.

  • Circadian control of metabolism is widespread. One well-studied example is starch metabolism control, in which the clock anticipates dawn and modulates the rate of nocturnal starch degradation such that starch is used efficiently through the night and not fully depleted prior to dawn, which would result in carbon starvation responses.

Abstract

The plant circadian clock coordinates the responses to multiple and often simultaneous environmental challenges that the sessile plant cannot avoid. These responses must be integrated efficiently into dynamic metabolic and physiological networks essential for growth and reproduction. Many of the output pathways regulated by the circadian clock feed back to modulate clock function, leading to the appreciation of the clock as a central hub in a sophisticated regulatory network. In this Review, we discuss the circadian regulation of growth, flowering time, abiotic and biotic stress responses, and metabolism, as well as why temporal 'gating' of these processes is important to plant fitness.

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Figure 1: Model of the Arabidopsis thaliana circadian clock.
Figure 2: The circadian system of plants.
Figure 3: Photoperiodic regulation of flowering initiation in Arabidopsis thaliana.
Figure 4: Circadian clock gating of abiotic stress response.
Figure 5: Circadian regulation of resistance to pathogens and herbivores.
Figure 6: Circadian regulation of starch degradation.

Change history

  • 13 October 2015

    In this article, the authors have updated Figure 1 by removing the repressive post-translational regulation arrow originally linking ZEITLUPE (ZTL) to the evening complex (EC), which is a multi-protein complex consisting of EARLY FLOWERING 4 (ELF4), ELF3 and LUX ARRHYTHMO (LUX). This alteration is because this regulatory relationship is not supported by the current literature. The authors apologize for this error.

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Acknowledgements

The authors thank three anonymous reviewers for their comments and apologize to those whose work has not been cited owing to length constraints. This work was supported by grants from the US National Science Foundation (IOS-1202779 to K.G. and IOS-0923752, IOS-1025965 and IOS-1257722 to C.R.M.) and from the Rural Development Administration, Republic of Korea (Next-Generation BioGreen 21 Programme, Systems and Synthetic Agrobiotech Center (PJ01106904 to C.R.M.)).

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PowerPoint slides

Glossary

Self-sustaining periodicity

Continued rhythmicity in the absence of environmental stimuli.

Entrainment

Setting of period and phase by external cues, termed zeitgeber ('time giver' in German), the strongest of which is light. Temperature cycles can also be effective zeitgebers.

Temperature compensation

The close maintenance of circadian periods within a physiological range at varying temperatures by buffering to compensate for changes in the rates of biochemical reactions.

Circadian clock

An endogenous time-keeping mechanism that requires approximately 24 hours to complete a single cycle.

Photoperiods

The duration of light in one day.

Free-running conditions

Experimental environment under constant light and temperature, permitting assessment of the endogenous periodicity and phase of a rhythm.

Period

The time to complete a single cycle under constant conditions of light and temperature.

Phase

The time in the circadian rhythm at which a particular rhythmic output occurs. Typically, acrophase (peak of the rhythm) is measured but trough, mid-rise and mid-fall are also used.

Phytochrome

Red (~650 nm) and far-red (~740 nm) light-absorbing photoreceptors. In Arabidopsis thaliana, phytochromes are encoded by a five-member gene family, PHYTOCHROME A (PHYA)–PHYE. The phytochrome apoproteins are covalently bound to a linear tetrapyrrole chromophore.

External coincidence

The coincidence of an internal rhythm driven by the circadian clock with external photoperiodic information. For example, on short days, CONSTANS (CO) mRNA and protein are synthesized after dusk; in the dark, CO is unstable and fails to accumulate. By contrast, on long days, CO mRNA accumulates before dusk, so newly translated CO is stabilized in the light and accumulates.

Florigens

Molecules (or molecular complexes) responsible for floral induction. Florigens are produced in the leaves and transmitted through the phloem to the shoot apical meristem of buds and growing tips.

Internal coincidence

The coincidence of two internal rhythms driven by the circadian clock. For example, GIGANTEA (GI) accumulates at about dusk on short days, whereas FLAVIN-BINDING KELCH REPEAT F-BOX 1 (FKF1) peaks after dark. However, under long-day conditions, the peaks of both proteins coincide in the late afternoon, enabling the accumulation of an FKF1–GI complex.

Long-day plant

A plant that exhibits a photoperiodic behaviour (for example, accelerated flowering) when the day length is greater than a threshold value.

Cryptochrome

(CRY). Blue-light-absorbing photoreceptors. In Arabidopsis thaliana, CRYs are encoded by two genes, CRY1 and CRY2. The CRY apoproteins are non-covalently bound to pterin and flavin chromophores, which absorb light at 380 nm and 450 nm, respectively.

Short-day plants

Plants that exhibit a photoperiodic behaviour (for example, accelerated flowering) when the day length is less than a threshold value.

Vernalization

A prolonged period of chilling that results in the acquisition or acceleration of the ability to flower.

Biotroph

A plant pathogen that does not kill the plant as part of the infection process, instead establishing a long-term feeding relationship with the living cells of the host.

Necrotrophic fungus

A fungal plant pathogen that kills plant cells as part of the infection process, feeding on the dead cells of the host.

Carbon partitioning

The distribution of carbon assimilates from photosynthetic tissues to non-photosynthetic organs.

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Greenham, K., McClung, C. Integrating circadian dynamics with physiological processes in plants. Nat Rev Genet 16, 598–610 (2015). https://doi.org/10.1038/nrg3976

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